Fetal growth restriction is a host specific response to infection with an impaired spiral artery remodeling-inducing strain of Porphyromonas gingivalis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
03 09 2020
03 09 2020
Historique:
received:
26
05
2020
accepted:
13
08
2020
entrez:
5
9
2020
pubmed:
5
9
2020
medline:
26
3
2021
Statut:
epublish
Résumé
Porphyromonas gingivalis is a periodontal pathogen implicated in a range of pregnancy disorders that involve impaired spiral artery remodeling (ISAR) with or without fetal growth restriction (FGR). Using a rodent periodontitis model, we assessed the ability of P. gingivalis to produce ISAR and FGR in Sprague Dawley (SD) and Wistar (WIS) rats. Both infected SD and WIS rats developed ISAR, but only WIS rats developed FGR despite both rat strains having equivalent microbial loads within the placenta. Neither maternal systemic inflammation nor placental (fetal) inflammation was a feature of FGR in WIS rats. Unique to infected WIS rats, was loss of trophoblast cell density within the junctional zone of the placenta that was not present in SD tissues. In addition, infected WIS rats had a higher proportion of junctional zone trophoblast cells positive for cytoplasmic high temperature requirement A1 (Htra1), a marker of cellular oxidative stress. Our results show a novel phenomenon present in P. gingivalis-induced FGR, with relevance to human disease since dysregulation of placental Htra1 and placental oxidative stress are features of preeclamptic placentas and preeclampsia with FGR.
Identifiants
pubmed: 32884071
doi: 10.1038/s41598-020-71762-9
pii: 10.1038/s41598-020-71762-9
pmc: PMC7471333
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14606Subventions
Organisme : NICHD NIH HHS
ID : R03 HD087633
Pays : United States
Références
Baek, K. J., Ji, S., Kim, Y. C. & Choi, Y. Association of the invasion ability of Porphyromonas gingivalis with the severity of periodontitis. Virulence 6, 274–281. https://doi.org/10.1080/21505594.2014.1000764 (2015).
doi: 10.1080/21505594.2014.1000764
pubmed: 25616643
pmcid: 4601282
Ibrahim, M. I. et al. Can Porphyromonas gingivalis be a novel aetiology for recurrent miscarriage?. Eur. J. Contracept. Reprod. Health Care 20, 119–127. https://doi.org/10.3109/13625187.2014.962651 (2015).
doi: 10.3109/13625187.2014.962651
pubmed: 25328050
Leon, R. et al. Detection of Porphyromonas gingivalis in the amniotic fluid in pregnant women with a diagnosis of threatened premature labor. J. Periodontol. 78, 1249–1255. https://doi.org/10.1902/jop.2007.060368 (2007).
doi: 10.1902/jop.2007.060368
pubmed: 17608580
Katz, J., Chegini, N., Shiverick, K. T. & Lamont, R. J. Localization of P. gingivalis in preterm delivery placenta. J. Dent. Res. 88, 575–578. https://doi.org/10.1177/0022034509338032 (2009).
doi: 10.1177/0022034509338032
pubmed: 19587165
pmcid: 3144059
Barak, S., Oettinger-Barak, O., Machtei, E. E., Sprecher, H. & Ohel, G. Evidence of periopathogenic microorganisms in placentas of women with preeclampsia. J. Periodontol. 78, 670–676. https://doi.org/10.1902/jop.2007.060362 (2007).
doi: 10.1902/jop.2007.060362
pubmed: 17397314
Swati, P., Thomas, B., Vahab, S. A., Kapaettu, S. & Kushtagi, P. Simultaneous detection of periodontal pathogens in subgingival plaque and placenta of women with hypertension in pregnancy. Arch. Gynecol. Obstet. https://doi.org/10.1007/s00404-011-2012-9 (2011).
doi: 10.1007/s00404-011-2012-9
pubmed: 21830010
Chaparro, A. et al. Porphyromonas gingivalis, Treponema denticola and toll-like receptor 2 are associated with hypertensive disorders in placental tissue: A case–control study. J. Periodontal. Res. https://doi.org/10.1111/jre.12074 (2013).
doi: 10.1111/jre.12074
pubmed: 23711357
Vanterpool, S. F. et al. Porphyromonas gingivalis within placental villous mesenchyme and umbilical cord stroma is associated with adverse pregnancy outcome. PLoS ONE 11, e0146157. https://doi.org/10.1371/journal.pone.0146157 (2016).
doi: 10.1371/journal.pone.0146157
pubmed: 26731111
pmcid: 4701427
Ao, M. et al. Dental Infection of Porphyromonas gingivalis induces preterm birth in mice. PLoS ONE 10, e0137249. https://doi.org/10.1371/journal.pone.0137249 (2015).
doi: 10.1371/journal.pone.0137249
pubmed: 26322971
pmcid: 4556457
Liang, S. et al. Periodontal infection with Porphyromonas gingivalis induces preterm birth and lower birth weight in rats. Mol. Oral. Microbiol. 33, 312–321. https://doi.org/10.1111/omi.12227 (2018).
doi: 10.1111/omi.12227
pubmed: 29754448
Phillips, P., Brown, M. B., Progulske-Fox, A., Wu, X. J. & Reyes, L. Porphyromonas gingivalis strain dependent inhibition of uterine spiral artery remodeling in the pregnant rat. Biol. Reprod. https://doi.org/10.1093/biolre/ioy119 (2018).
doi: 10.1093/biolre/ioy119
pubmed: 29788108
pmcid: 6297315
Reyes, L. et al. Porphyromonas gingivalis and adverse pregnancy outcome. J. Oral. Microbiol. 10, 1374153. https://doi.org/10.1080/20002297.2017.1374153 (2018).
doi: 10.1080/20002297.2017.1374153
pubmed: 29291034
Lin, D. et al. Porphyromonas gingivalis infection during pregnancy increases maternal tumor necrosis factor alpha, suppresses maternal interleukin-10, and enhances fetal growth restriction and resorption in mice. Infect. Immun. 71, 5156–5162 (2003).
doi: 10.1128/IAI.71.9.5156-5162.2003
Lin, D. et al. Porphyromonas gingivalis infection in pregnant mice is associated with placental dissemination, an increase in the placental Th1/Th2 cytokine ratio, and fetal growth restriction. Infect. Immun. 71, 5163–5168 (2003).
doi: 10.1128/IAI.71.9.5163-5168.2003
Michelin, M., Teixeira, S., Ando-Suguimoto, E., Lucas, S. & Mayer, M. Porphyromonas gingivalis infection at different gestation periods on fetus development and cytokines profile. Oral. Dis. 18, 648–654. https://doi.org/10.1111/j.1601-0825.2012.01917.x (2012).
doi: 10.1111/j.1601-0825.2012.01917.x
pubmed: 22471815
Brosens, I., Pijnenborg, R., Vercruysse, L. & Romero, R. The, “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am. J. Obstet. Gynecol. 204, 193–201. https://doi.org/10.1016/j.ajog.2010.08.009 (2011).
doi: 10.1016/j.ajog.2010.08.009
pubmed: 21094932
Brosens, I., Benagiano, M., Puttemans, P., D’Elios, M. M. & Benagiano, G. The placental bed vascular pathology revisited: A risk indicator for cardiovascular disease. J Matern. Fetal. Neonatal. Med. https://doi.org/10.1080/14767058.2017.1409718 (2017).
doi: 10.1080/14767058.2017.1409718
pubmed: 29172831
Brosens, I., Pijnenborg, R. & Benagiano, G. Defective myometrial spiral artery remodelling as a cause of major obstetrical syndromes in endometriosis and adenomyosis. Placenta 34, 100–105. https://doi.org/10.1016/j.placenta.2012.11.017 (2013).
doi: 10.1016/j.placenta.2012.11.017
pubmed: 23232321
Kim, Y. M. et al. The frequency of acute atherosis in normal pregnancy and preterm labor, preeclampsia, small-for-gestational age, fetal death and midtrimester spontaneous abortion. J. Matern. Fetal. Neonatal. Med. https://doi.org/10.3109/14767058.2014.976198 (2014).
doi: 10.3109/14767058.2014.976198
pubmed: 25308204
pmcid: 4427552
Fetal Growth Restriction. ACOG Practice Bulletin No. 204. Obstet. Gynecol. 133, e97–e109. https://doi.org/10.1097/aog.0000000000003070 (2019).
doi: 10.1097/aog.0000000000003070
Sharma, D., Shastri, S. & Sharma, P. Intrauterine growth restriction: Antenatal and postnatal aspects. Clin. Med. Insights: Pediatrics 10, CMPed.S40070. https://doi.org/10.4137/CMPed.S40070 (2016).
doi: 10.4137/CMPed.S40070
Malhotra, A. et al. Neonatal Morbidities of Fetal Growth Restriction: Pathophysiology and Impact. Front. Endocrinol. https://doi.org/10.3389/fendo.2019.00055 (2019).
doi: 10.3389/fendo.2019.00055
Walkenhorst, M. S. et al. A uniquely altered oral microbiome composition was observed in pregnant rats with Porphyromonas gingivalis induced periodontal disease. Front. Cell Infect. Microbiol. 10, 92. https://doi.org/10.3389/fcimb.2020.00092 (2020).
doi: 10.3389/fcimb.2020.00092
pubmed: 32211345
pmcid: 7069352
Supanji, S., Shimomachi, M., Hasan, M. Z., Kawaichi, M. & Oka, C. HtrA1 is induced by oxidative stress and enhances cell senescence through p38 MAPK pathway. Exp. Eye Res. 112, 79–92. https://doi.org/10.1016/j.exer.2013.04.013 (2013).
doi: 10.1016/j.exer.2013.04.013
pubmed: 23623979
Zurawa-Janicka, D. et al. Structural insights into the activation mechanisms of human HtrA serine proteases. Arch. Biochem. Biophys. 621, 6–23. https://doi.org/10.1016/j.abb.2017.04.004 (2017).
doi: 10.1016/j.abb.2017.04.004
pubmed: 28396256
Schoots, M. H., Gordijn, S. J., Scherjon, S. A., van Goor, H. & Hillebrands, J. L. Oxidative stress in placental pathology. Placenta 69, 153–161. https://doi.org/10.1016/j.placenta.2018.03.003 (2018).
doi: 10.1016/j.placenta.2018.03.003
pubmed: 29622278
Ajayi, F. et al. Elevated expression of serine protease HtrA1 in preeclampsia and its role in trophoblast cell migration and invasion. Am. J. Obstet. Gynecol. 199(557), e551–e510. https://doi.org/10.1016/j.ajog.2008.04.046 (2008).
doi: 10.1016/j.ajog.2008.04.046
Lorenzi, T. et al. Expression patterns of two serine protease HtrA1 forms in human placentas complicated by preeclampsia with and without intrauterine growth restriction. Placenta 30, 35–40. https://doi.org/10.1016/j.placenta.2008.10.016 (2009).
doi: 10.1016/j.placenta.2008.10.016
pubmed: 19056122
Brosens, I., Puttemans, P. & Benagiano, G. Placental bed research: I. The placental bed: From spiral arteries remodeling to the great obstetrical syndromes. Am. J. Obstet. Gynecol. 221, 437–456. https://doi.org/10.1016/j.ajog.2019.05.044 (2019).
doi: 10.1016/j.ajog.2019.05.044
pubmed: 31163132
Nardozza, L. M. et al. Fetal growth restriction: Current knowledge. Arch. Gynecol. Obstet. 295, 1061–1077. https://doi.org/10.1007/s00404-017-4341-9 (2017).
doi: 10.1007/s00404-017-4341-9
pubmed: 28285426
Romero, A., Villamayor, F., Grau, M. T., Sacristán, A. & Ortiz, J. A. Relationship between fetal weight and litter size in rats: Application to reproductive toxicology studies. Reprod. Toxicol. 6, 453–456. https://doi.org/10.1016/0890-6238(92)90009-I (1992).
doi: 10.1016/0890-6238(92)90009-I
pubmed: 1463926
Ahokas, R. A., Lahaye, E. B., Anderson, G. D. & Lipshitz, J. Effect of maternal dietary restriction on fetal growth and placental transfer of alpha-amino isobutyric acid in rats. J. Nutr. 111, 2052–2058. https://doi.org/10.1093/jn/111.12.2052 (1981).
doi: 10.1093/jn/111.12.2052
pubmed: 7310531
Kim, C. J., Romero, R., Chaemsaithong, P. & Kim, J. S. Chronic inflammation of the placenta: Definition, classification, pathogenesis, and clinical significance. Am. J. Obstet. Gynecol. 213, S53-69. https://doi.org/10.1016/j.ajog.2015.08.041 (2015).
doi: 10.1016/j.ajog.2015.08.041
pubmed: 26428503
pmcid: 4782598
Burton, G. J. & Jauniaux, E. Pathophysiology of placental-derived fetal growth restriction. Am. J. Obstet. Gynecol. 218, S745-s761. https://doi.org/10.1016/j.ajog.2017.11.577 (2018).
doi: 10.1016/j.ajog.2017.11.577
pubmed: 29422210
Goldenberg, R. L. et al. The Alabama Preterm Birth Study: Diffuse decidual leukocytoclastic necrosis of the decidua basalis, a placental lesion associated with preeclampsia, indicated preterm birth and decreased fetal growth. J. Matern. Fetal. Neonatal. Med. 20, 391–395. https://doi.org/10.1080/14767050701236365 (2007).
doi: 10.1080/14767050701236365
pubmed: 17674243
Kovo, M. et al. The placental component in early-onset and late-onset preeclampsia in relation to fetal growth restriction. Prenat. Diagn. 32, 632–637. https://doi.org/10.1002/pd.3872 (2012).
doi: 10.1002/pd.3872
pubmed: 22565848
Dealtry, G. B., Clark, D. E., Sharkey, A., Charnock-Jones, D. S. & Smith, S. K. Expression and localization of the Th2-type cytokine interleukin-13 and its receptor in the placenta during human pregnancy. Am. J. Reprod. Immunol. 40, 283–290. https://doi.org/10.1111/j.1600-0897.1998.tb00419.x (1998).
doi: 10.1111/j.1600-0897.1998.tb00419.x
pubmed: 9784801
Amash, A. et al. The expression of interleukin-15 and interleukin-18 by human term placenta is not affected by lipopolysaccharide. Eur. Cytokine Netw. 18, 188–194. https://doi.org/10.1684/ecn.2007.0102 (2007).
doi: 10.1684/ecn.2007.0102
pubmed: 17964972
Huang, X., Huang, H., Dong, M., Yao, Q. & Wang, H. Serum and placental interleukin-18 are elevated in preeclampsia. J. Reprod. Immunol. 65, 77–87. https://doi.org/10.1016/j.jri.2004.09.003 (2005).
doi: 10.1016/j.jri.2004.09.003
pubmed: 15694969
Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108 (2008).
doi: 10.1038/nprot.2008.73
Zong, L. et al. High temperature requirement A1 in placental tissues and serum from pre-eclamptic pregnancies with or without fetal growth restriction. Arch. Med. Sci. 9, 690–696. https://doi.org/10.5114/aoms.2013.34989 (2013).
doi: 10.5114/aoms.2013.34989
pubmed: 24049530
pmcid: 3776172
Wijayarathna, R. & de Kretser, D. M. Activins in reproductive biology and beyond. Hum. Reprod. Update 22, 342–357. https://doi.org/10.1093/humupd/dmv058 (2016).
doi: 10.1093/humupd/dmv058
pubmed: 26884470
Clawson, G. A., Bui, V., Xin, P., Wang, N. & Pan, W. Intracellular localization of the tumor suppressor HtrA1/Prss11 and its association with HPV16 E6 and E7 proteins. J. Cell Biochem. 105, 81–88. https://doi.org/10.1002/jcb.21804 (2008).
doi: 10.1002/jcb.21804
pubmed: 18452160
Tossetta, G. et al. High temperature requirement A1 and fibronectin: Two possible players in placental tissue remodelling. Eur. J. Histochem. 60, 2724. https://doi.org/10.4081/ejh.2016.2724 (2016).
doi: 10.4081/ejh.2016.2724
pubmed: 28076935
pmcid: 5134679
Fischer, L. A., Bittner-Eddy, P. D. & Costalonga, M. Fetal weight outcomes in C57BL/6J and C57BL/6NCrl mice after oral colonization with Porphyromonas gingivalis. Infect. Immun. https://doi.org/10.1128/iai.00280-19 (2019).
doi: 10.1128/iai.00280-19
pubmed: 31331955
pmcid: 6759314
Becker, K. J. Strain-related differences in the immune response: Relevance to human stroke. Transl. Stroke Res. 7, 303–312. https://doi.org/10.1007/s12975-016-0455-9 (2016).
doi: 10.1007/s12975-016-0455-9
pubmed: 26860504
pmcid: 4929040
Reyes, L., Reinhard, M., O’Donell, L. J., Stevens, J. & Brown, M. B. Rat strains differ in susceptibility to Ureaplasma parvum-induced urinary tract infection and struvite stone formation. Infect. Immun. 74, 6656–6664. https://doi.org/10.1128/IAI.00984-06 (2006).
doi: 10.1128/IAI.00984-06
pubmed: 16982825
pmcid: 1698052
Reyes, L., Steiner, D. A., Hutchison, J., Crenshaw, B. & Brown, M. B. Mycoplasma pulmonis genital disease: Effect of rat strain on pregnancy outcome. Comp. Med. 50, 622–627 (2000).
pubmed: 11200568
Belanger, M. et al. Colonization of maternal and fetal tissues by Porphyromonas gingivalis is strain-dependent in a rodent animal model. Am. J. Obstet. Gynecol. 199(86), e81-87. https://doi.org/10.1016/j.ajog.2007.11.067 (2008).
doi: 10.1016/j.ajog.2007.11.067
Sanz, M., Kornman, K. & Working group 3 of joint, E. F. P. A. A. P. w. Periodontitis and adverse pregnancy outcomes: Consensus report of the joint EFP/AAP workshop on periodontitis and systemic diseases. J. Clin. Periodontol. 40(Suppl 14), S164–S169. https://doi.org/10.1111/jcpe.12083 (2013).
Kim, C. J. et al. Acute chorioamnionitis and funisitis: Definition, pathologic features, and clinical significance. Am. J. Obstet. Gynecol. 213, S29-52. https://doi.org/10.1016/j.ajog.2015.08.040 (2015).
doi: 10.1016/j.ajog.2015.08.040
pubmed: 26428501
pmcid: 4774647
Kaufmann, P., Huppertz, B. & Frank, H. G. The fibrinoids of the human placenta: Origin, composition and functional relevance. Ann. Anat. 178, 485–501. https://doi.org/10.1016/s0940-9602(96)80102-6 (1996).
doi: 10.1016/s0940-9602(96)80102-6
pubmed: 9010564
Burton, G. J. & Jauniaux, E. Pathophysiology of placental-derived fetal growth restriction. Am. J. Obstet. Gynecol. 218, S745–S761. https://doi.org/10.1016/j.ajog.2017.11.577 (2018).
doi: 10.1016/j.ajog.2017.11.577
pubmed: 29422210
Ness, R. B. & Sibai, B. M. Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia. Am. J. Obstet. Gynecol. 195, 40–49. https://doi.org/10.1016/j.ajog.2005.07.049 (2006).
doi: 10.1016/j.ajog.2005.07.049
pubmed: 16813742
Ilievski, V. et al. Experimental periodontitis results in prediabetes and metabolic alterations in brain, liver and heart: Global untargeted metabolomic analyses. J. Oral Biol. (Northborough) https://doi.org/10.13188/2377-987x.1000020 (2016).
doi: 10.13188/2377-987x.1000020
Kato, T. et al. Oral administration of Porphyromonas gingivalis alters the gut microbiome and serum metabolome. mSphere https://doi.org/10.1128/mSphere.00460-18 (2018).
doi: 10.1128/mSphere.00460-18
pubmed: 30333180
pmcid: 6193602
Nakajima, M. et al. Oral administration of P. gingivalis induces dysbiosis of gut microbiota and impaired barrier function leading to dissemination of enterobacteria to the liver. PLoS ONE 10, e0134234. https://doi.org/10.1371/journal.pone.0134234 (2015).
doi: 10.1371/journal.pone.0134234
pubmed: 26218067
pmcid: 4517782
Jiang, J. et al. Overexpression of HTRA1 leads to down-regulation of fibronectin and functional changes in RF/6A cells and HUVECs. PLoS ONE 7, e46115–e46115. https://doi.org/10.1371/journal.pone.0046115 (2012).
doi: 10.1371/journal.pone.0046115
pubmed: 23056244
pmcid: 3466263
Liu, C. et al. Elevated HTRA1 and HTRA4 in severe preeclampsia and their roles in trophoblast functions. Mol. Med. Rep. 18, 2937–2944. https://doi.org/10.3892/mmr.2018.9289 (2018).
doi: 10.3892/mmr.2018.9289
pubmed: 30015931
Zurawa-Janicka, D. et al. Changes in expression of serine proteases HtrA1 and HtrA2 during estrogen-induced oxidative stress and nephrocarcinogenesis in male Syrian hamster. Acta Biochim. Pol. 55, 9–19 (2008).
doi: 10.18388/abp.2008_3123
Nie, G., Li, Y. & Salamonsen, L. A. Serine protease HtrA1 is developmentally regulated in trophoblast and uterine decidual cells during placental formation in the mouse. Dev. Dyn. 233, 1102–1109. https://doi.org/10.1002/dvdy.20399 (2005).
doi: 10.1002/dvdy.20399
pubmed: 15861393
Tong, Y. et al. LOC387715/HTRA1 gene polymorphisms and susceptibility to age-related macular degeneration: A HuGE review and meta-analysis. Mol. Vis. 16, 1958–1981 (2010).
pubmed: 21031019
pmcid: 2956667
Dai, Z., Wu, Z., Hang, S., Zhu, W. & Wu, G. Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction. Mol. Hum. Reprod. 21, 389–409. https://doi.org/10.1093/molehr/gav003 (2015).
doi: 10.1093/molehr/gav003
pubmed: 25609213
Kaufmann, P., Black, S. & Huppertz, B. Endovascular trophoblast invasion: Implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 69, 1–7. https://doi.org/10.1095/biolreprod.102.014977 (2003).
doi: 10.1095/biolreprod.102.014977
pubmed: 12620937
Cotechini, T. et al. Inflammation in rat pregnancy inhibits spiral artery remodeling leading to fetal growth restriction and features of preeclampsia. J. Exp. Med. 211, 165–179. https://doi.org/10.1084/jem.20130295 (2014).
doi: 10.1084/jem.20130295
pubmed: 24395887
pmcid: 3892976
Geusens, N. et al. Changes in endovascular trophoblast invasion and spiral artery remodelling at term in a transgenic preeclamptic rat model. Placenta 31, 320–326. https://doi.org/10.1016/j.placenta.2010.01.011 (2010).
doi: 10.1016/j.placenta.2010.01.011
pubmed: 20144482